Abstract
Sensory systems evolve in the ecological niches each species is occupying. Accordingly, encoding of natural stimuli by sensory neurons is expected to be adapted to the statistics of these stimuli. For a direct quantification of sensory scenes we tracked natural communication behavior of male and female weakly electric fish, Apteronotus rostratus, in their Neotropical rainforest habitat with high spatio-temporal resolution over several days. In the context of courtship we observed large quantities of electrocommunication signals. Echo responses, acknowledgment signals, and their synchronizing role in spawning demonstrated the behavioral relevance of these signals. In both courtship and aggressive contexts, we observed robust behavioral responses in stimulus regimes that have so far been neglected in electrophysiological studies of this well characterized sensory system and that are well beyond the range of known best frequency and amplitude tuning of the electroreceptor afferents' firing rate modulation. Our results emphasize the importance of quantifying sensory scenes derived from freely behaving animals in their natural habitats for understanding the function and evolution of neural systems.
Significance statement
The processing mechanisms of sensory systems have evolved in the context of the natural lives of organisms. To understand the functioning of sensory systems therefore requires probing them in the stimulus regimes they evolved in. We took advantage of the continuously generated electric fields of weakly electric fish to explore electrosensory stimulus statistics in their natural Neotropical habitat. Unexpectedly, many of the electrocommunication signals recorded during courtship, spawning, and aggression had much smaller amplitudes or higher frequencies than stimuli used so far in neurophysiological characterizations of the electrosensory system. Our results demonstrate that quantifying sensory scenes derived from freely behaving animals in their natural habitats is essential to avoid biases in the choice of stimuli used to probe brain function.
Footnotes
The authors declare no competing financial interests.
Supported by the BMBF Bernstein Award Computational Neuroscience 01GQ0802 to J.B., a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to RK, and a Short Time Fellowship to J.H. from the Smithonian Tropical Research Institute. We thank Hans Reiner Polder and Jürgen Planck from npi electronic GmbH for designing the amplifier, Sophie Picq, Diana Sharpe, Luis de León Reyna, Rigoberto González, Eldredge Bermingham, the staff from the Smithsonian Tropical Research Institute, and the Emberá community of Peña Bijagual for their logistical support, Fabian Sinz for advice on the analysis, and Ulrich Schnitzler and Janez Presern for comments on the manuscript.
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